The Context of Dietary Variation in Cercopithecus Diana in the Ivory Coast’S Taï National Park

Home , Cercopithecini, Diana monkey, Guenon, Oldfieldia, Roloway monkey

The Context of Dietary Variation in Cercopithecus diana in the Ivory Coast’s Taï National Park

THESIS

Presented in Partial Fulfillment of the Requirements for the Degree Master of Arts in the Graduate School of The Ohio State University

Erin Elizabeth Kane

Graduate Program in Anthropology

The Ohio State University

2012

Master's Examination Committee:

Professor Debra Guatelli-Steinberg

Professor Dawn Kitchen

Professor W. Scott McGraw, Advisor

Copyrighted by

Erin Elizabeth Kane

2012

Abstract

There is increased recognition of the capacity for intraspecific dietary variation; however, previous studies of this phenomenon in Cercopithecus have focused only on guenons from a handful of sites. The lack of comparative and longitudinal data for West

African guenons, including the Diana monkey Cercopithecus diana, inhibits our ability to assess habitat requirements, identify keystone resources, and make informed conservation decisions. Here, I present 5 years of feeding data on four Diana monkey groups ranging within the Ivory Coast’s Taï Forest. Food scans taken every 30 minutes were used to generate feeding profiles, which are interpreted through five years of phonological data collected on feeding trees.

I find significant inter-annual and monthly dietary variation in the Diana monkey diet. Though not statistically tested, monthly consumption of a particular fruit seems to be related to its abundance as shown through its phonological profile. Diana monkeys depend primarily on two fruit species, Sacoglottis gabonensis and Dialium aubrevillei, which are available during opposite seasons. Sacoglottis gabonensis is consumed during the period of lowest fruit abundance, Dialium aubrevillei during the period of highest fruit abundance. Though this would suggest that the concept of fallback foods may be relevant, I find no evidence to suggest that fallback foods provide a useful mechanism for explaining the Diana monkey diet. ii

Though there is significant temporal variation in the Diana monkey diet, Diana monkey group diets are remarkably similar. At Taï, Diana monkey diets comprise about

70% fruit, 25% insects, 4.6% leaves, and 0.4% other material. This is the most frugivorous of Diana monkey populations studied. Additionally, Diana monkeys are among the most frugivorous of guenon species whose diet is well studied.

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Acknowledgments

I would like to thank my advisor, Dr. Scott McGraw, and my thesis committee, Dr.

Debbie Guatelli-Steinberg and Dr. Dawn Kitchen, for their support and feedback throughout my master’s. I also gratefully acknowledge the field assistants of Taï Monkey

Project for their work collecting the data I was able to use to develop this thesis.

Vita

June 2006 ...... Manchester Central High School

2009...... B. A. Anthropology, Washington University

in St. Louis

2011 to present ...... Graduate Teaching Associate, Department

of Anthropology, The Ohio State University

Publications

E. Kane, E. A. Bitty, W.S. McGraw. 2011. Monthly, Seasonal and Annual Dietary

Variation in Cercopithecus diana in the Ivory Coast’s Taï National Park.

American Journal of Primatology 73(S1): 60.

Fields of Study

Major Field: Anthropology

Table of Contents

Abstract ...... ii

Acknowledgments...... iv

Vita ...... v

List of Tables ...... ix

List of Figures ...... xi

Chapter 1: Introduction ...... 1

Chapter 2: Methods ...... 7

Study Site ...... 7

Study Species ...... 9

Behavioral Sampling Methods ...... 10

Phenological Sampling Methods ...... 11

Statistical Methods ...... 12

Chapter 3: Results ...... 14

Group Diet ...... 14

Temporal Variability ...... 15

Annual Dietary Variation ...... 15

Seasonal Dietary Variation ...... 16

Monthly Diet...... 17

Dietary Variation Across Forest Strata ...... 20

Age- and Sex-ClassVariation ...... 21

Interdemic Comparisons ...... 22

Interpopulation Comparisons ...... 23

Interspecies Comparisons ...... 23

Chapter 4: Discussion and Conclusions ...... 25

Group Variability ...... 25

Temporal Variability ...... 27

Annual Dietary Variation ...... 27

Seasonal Dietary Variation ...... 28

Monthly Dietary Variation ...... 29

Diana Monkeys and Fallback Foods ...... 30

Dietary Variation Between Forest Strata ...... 31

Dietary Variation Between Age- and Sex-Classes ...... 32

Interdemic Dietary Variation ...... 33

Interpopulational Dietary Variation ...... 33

vii

Interspecies Dietary Variation ...... 34

Directions For Further Study...... 35

Conclusions ...... 36

References ...... 38

Appendix A: Figures ...... 43

Appendix B: Tables ...... 71

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List of Tables

Table 1. Sampling effort over the duration of this study ...... 71

Table 2. Total group consumption of gross dietary components ...... 71

Table 3. Total group consumption of eight most frequently consumed plant parts ...... 72

Table 4. Annual consumption of fruit, insects, leaves, and other material from 2005-2008.

...... 72

Table 5. Annual consumption of the eight most frequently consumed plant parts from

2005-2008 ...... 73

Table 6. Seasonal consumpstion of eight most frequently consumed plant parts ...... 73

Table 7. Monthly consumption of fruit, insects, leaves, and other material ...... 74

Table 8. Monthly consumption of eight most frequently consumed plant parts...... 75

Table 9. Consumption of fruit, leaves, and insects across forest strata...... 76

Table 10. Consumption of eight most frequently consumed plant parts across forest strata

...... 76

Table 11. Consumption of fruit, insects, and leaves by adult females, adult males, and subadults ...... 77

Table 12. Consumption of eight most frequently consumed plant parts by adult females, adult males, and subadults ...... 77

Table 13. Consumption of fruit, insects, leaves, and other material by the contiguous groups (Diana 1, Diana 2, Diana 3) and the northern group (Diana N) ...... 77

Table 14. Consumption of the eight most frequently consumed plant parts by the contiguous groups (Diana 1, Diana 2, Diana 3) and the northern group (Diana N)...... 78

Table 15. Consumption of fruit, leaves, insects, and other material across Cercopithecus diana populations (Galat and Galat-Luong 1978, Oates and Whitesides 1990, Buzzard

2006, Curtin 2002, *this study)...... 78

Table 16. Consumption of fruit, leaves, insects, and other material by multiple guenon species (Chapman et al. 2002, *this study)...... 79

List of Figures

Figure 1. The location of the Taï Forest...... 43

Figure 2. Mean monthly rainfall and average minimum and maximum temperatures in the

Taï Forest (Anderson et al. 2005)...... 44

Figure 3. Cercopithecus diana eating Sacoglottis gabonensis fruit at the Taï National

Park. Picture taken by Scott McGraw...... 44

Figure 4. Strata levels in the Taï Forest, from McGraw 1998...... 45

Figure 5. Total group consumption of gross dietary components ...... 46

Figure 6. The fruit of Dialium aubrevillei (Hawthorne and Gyakari 2006) ...... 47

Figure 7. The seeds of Sacoglottis gabonensis (Hawthorne and Gyakari 2006) ...... 48

Figure 8. The fruit of Scytopetalum tieghemii (Hawthorne and Gyakari 2006) ...... 49

Figure 9. The fruit of Diospyros soubreana (Hawthorne and Jongkind 2006) ...... 49

Figure 10. The fruit of Diospyros mannii (Hawthorne and Jongkind 2006)...... 50

Figure 11. The fruit of Parinari excelsa (Hawthorne and Gyakari 2006)...... 50

Figure 12. Leaves of Craterispermum caudatum (Hawthorne and Jongkind 2006) ...... 51

Figure 13. Total group consumption of the eight most frequently consumed plant parts. 52

Figure 14. Annual consumption of leaves, insects, fruits, and other dietary components from 2005-2008 ...... 53

Figure 15. Annual consumption of the eight most frequently consumed plant parts ...... 54 xi

Figure 16. Seasonal consumption of fruit, insects, leaves, and other material ...... 54

Figure 17. Seasonal consumption of the eight most frequently consumed plant parts ..... 55

Figure 18. Monthly consumption of fruit, insects, leaves, and other material...... 56

Figure 19. Mean monthly rainfall and monthly consumption of fruit, insects, leaves, and other material during 2008 ...... 56

Figure 20. Monthly consumption of the eight most frequently consumed plant parts ..... 57

Figure 21. Monthly consumption and phenology of Sacoglottis gabonensis and Dialium aubrevillei ...... 58

Figure 22. Monthly consumption and phenology of Scytopetalum tieghemii ...... 59

Figure 23. Monthly consumption and phenology of Oldfieldia africana ...... 59

Figure 24. Monthly consumption and phenology of Craterispermum caudatum ...... 60

Figure 25. Monthly consumption and phenology of Parinari excelsa ...... 61

Figure 26. Monthly consumption and phenology of Diospyros soubreana ...... 62

Figure 27. Consumption of fruit, insect, and leaves in each forest strata ...... 63

Figure 28. Consumption of eight most frequently consumed plant parts in each forest strata ...... 64

Figure 29.Consumption of leaves, insects, and fruit by adult females, adult males, and subadults...... 65

Figure 30. Consumption of eight most important plant parts by adult females, adult males, and subadults ...... 65

Figure 31. Interdemic comparison of fruit, insects, leaf and other material consumption 66

Figure 32. Interdemic consumption of eight most frequently consumed plant parts...... 67

xii

Figure 33. Consumption of fruit, insects, leaves, and other material by Diana monkeys at different sites across their range ...... 68

Figure 34 Proportion of fruit, insects, leaves, and other material in the diet of

Cercopithecus diana and five other guenons (Chapman et al. 2002) ...... 69

Figure 35. Fruit abundance in the Taï Forest between February 1997 and January 2000

(Anderson et al. 2005) ...... 69

Figure 36. Frequency of behaviors performed at each level of the forest ...... 70

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Chapter 1: Introduction

Although characterizing the diet of primates has long been a goal of primatologists (Struhsaker 1967, Clutton-Brock 1977, Gautier-Hion 1980) it is only fairly recently that primates’ capacity for intraspecific dietary variation has been recognized

(Chapman and Chapman 1990). Consequently, the underlying mechanisms of this variation are poorly understood. However, some of the mechanisms which may drive intraspecific dietary variation have been particularly well studied through the lens of polyspecific associations between members of the genus Cercopithecus, with an emphasis on understanding niche differentiation in closely related primates. These include dietary shifts due to interannual, seasonal, and monthly fluctuations in fruit availability (Gautier-Hion 1980, Chapman and Chapman 1990, Tutin and Fernandez

1993), the effects of age and sex class on diet (Cords 1986a), both direct and scramble competition (Lambert 2002) and differential space use (Leite et al 2006, Buzzard 2006).

To varying degrees, these mechanisms may explain patterns of intraspecific dietary variation; however, their roles and relative importance remain obscured.

Understanding the interaction of these mechanisms allows us to understand the consequences of the selective pressures under which primate species evolved their dietary strategies, and how these might differ among species with divergent dietary strategies.

Additionally, evaluating the role of environmental variation in primate diets is critical to 1 the successful conservation of increasingly vulnerable animals, especially as global climate change affects seasonal patterns of rainfall and forest productivity worldwide

(Thomas et al. 2004, Zelazowski et al. 2011).

Studies of colobus monkeys (Procolobus tephrosceles, Colobus guereza) in

Kibale, Uganda, show that these folivorous primates have diets which vary significantly both temporally and spatially, to the extent that interdemic variation can be greater than interspecific variation (Chapman and Chapman 1999, Harris and Chapman 2007).

Complementing these studies and extending analyses of dietary variation to frugivorous primates, a meta-analysis of dietary variation in Cercopithecus monkeys compared the diets of six guenon species to assess the degree of intergroup, interdemic, interpopulational, and interspecific dietary variation (Chapman et al. 2002). This meta- analysis combined data from long-term studies of Cercopithecus representing three superspecies (cephus, nictitans,and mona), all of which are arboreal frugivores that supplement their diet with young leaves and insects.

Chapman and colleagues’ analyses (2002) showed that sympatric groups of the same species frequently ate diets which, though very similar in gross content (percentage of fruit, leaves, insect matter, and other materials), differed in the specific plants consumed. Populations of the same species in different forests ate diets that tended to be more similar to sympatric groups of other species than to conspecifics in other forests. In this analysis, all guenons supplemented their diet with young leaves. The mean proportion of fruit in the diet ranged from 46.65%-64.70%. Leaf consumption ranged from 7.13% to 23.93%; insect consumption from 11.30% to 23.71%. Studies were

2 conducted across East and Central Africa, at Kakamega Forest (Kenya,) Kibale National

Park (Uganda), three sites in Central Gabon, and Salonga National Park (Democratic

Republic of Congo). No species of guenon occurring west of Gabon was included in this analysis, nor have any been included in other analyses of intraspecific dietary variation.

Present Study

In this study, I assess the capacity for dietary variation in a rare frugivorous West

African cercopithecine. I identify potential correlates of dietary variation, and clarify ecological requirements for a species which is central to its primate community through an analysis of feeding data of four groups of Diana monkeys (Cercopithecus diana) collected between 2004-2009. As arboreal frugivores supplementing their diet primarily with insects and mature leaves (Buzzard 2006), Diana monkeys offer a counterpoint to extensive analyses of dietary variation in folivorous primates (Chapman and Chapman

1999, Harris and Chapman 2007) as well as an expansion of the meta-analysis of East and Central African guenons who supplement their frugivorous diet with insects and young leaves (Chapman et al. 2002). Because data collection spanned five years, this study also provides an excellent opportunity to test the magnitude of temporal variation in frugivorous primates, something that has not been adequately studied previously

(Chapman et al. 2002).

Though Diana monkeys are relatively poorly known compared to Eastern and

Central African guenons, years of study in the Ivory Coast’s Taï Forest allow multiple inter-annual dietary comparisons (Galat and Galat-Luong 1978, Buzzard 2006). A two- year study at Tiwai Island in Sierra Leone (Oates and Whiteside 1990) and a study of the

Diana monkey subspecies C. diana roloway in Ghana (Curtin 2004) also allow comparisons of Diana monkey diets across forests. Additionally, Taï is an excellent location to study the effects of seasonality on primate diets because it experiences four seasons differentiated by substantial variation in temperature and rainfall: a long dry season (November-March), long wet season (April-June), short dry season (July-August), and short wet season (September-October) (Anderson et al 2005). Fruit availability peaks during the long dry season (from November to March), while leaf flushing peaks at the end of the long dry season and beginning of the long wet season (Anderson et al. 2005).

In this paper, I first test the null hypothesis that Diana monkey groups at Taï show no intergroup dietary variation. I predict that there will be significant variation in diets between groups. The intense competitive regime of Diana monkeys at Taï (McGraw et al.

2002) suggests that C. diana groups will have different diets as some groups more successfully defend access to patchy fruit trees which are unequally distributed throughout the forest (Wrangham 1980, Buzzard 2006). Diana monkeys at Taï have notably high levels of female-driven intergroup aggression (McGraw et al. 2002, Hill

1994), females have relatively large canines, a low degree of sexual dimorphism (Plavcan

1990), and are philopatric (Buzzard and Eckardt 2007). Diana monkeys seem to exemplify Wrangham’s model (1980) in which philopatric females exhibit high rates of inter-group aggression in an attempt to monopolize patchily distributed, defendable resources. If Diana monkey aggression is indeed linked to the successful monopolization of high quality resources, I expect different diets, perhaps with different nutritional value, between contiguous groups that frequently have these aggressive encounters.

Next, I test the null hypothesis that the Diana monkey diet at Taï will not vary in its composition annually, seasonally, or monthly. I predict that, due to annual differences in rainfall (Anderson 2005), there will be inter-annual dietary variation. Due to seasonal variation in fruit, leaf, and flower availability, as well as temporal variation in rainfall

(Anderson 2005), I predict that diets also vary seasonally and monthly.

Next, I test the null hypothesis that Diana monkeys eat the same foods across all forest strata. I predict that diets will vary at each level of the forest. Vertical stratification is an important aspect of niche differentiation among the guenons at Taï (Buzzard 2006), and while Diana monkeys spend much of their time in the upper levels of the forest

(Buzzard 2006), they forage in all levels of the canopy (McGraw 1998). That different foods are available depending upon where in a tree a particular group spends its time is an important property of niche differentiation for the formation of polyspecific associations, and I expect that foraging at different forest levels will lead to significantly different foods consumed in each strata.

I next test the null hypothesis that Diana monkeys of different age- and sex- classes have the same diets. I predict that diets will differ across age- and sex-class, and test this specifically for adult males, adult females, and subadults. Dietary variation between age- and sex-classes is recognized in several guenon species (Gautier-Hion

1980, Cords 1986). Guenons in polyspecific associations in Kakamega Forest had diets which were more similar to individuals of the same age- and sex- class from different species than conspecifics of other age- or sex-classes (Cords 1986), and I expect Diana monkeys will follow a similar pattern.

Finally, I place results from this study into the broader context of interdemic variation, interpopulation variation and interspecific variation. I test the null hypothesis that Diana monkeys will not show interdemic dietary variation by comparing three contiguous groups to a fourth group located at the same site, five kilometers away. I predict that there will be significant interdemic dietary variation. Butynski (1990) showed that even a distance of twelve kilometers was enough to show greater dietary differences between contiguous and distant groups than contiguous groups. Though not statistically tested, I compare Diana monkey diets from studies at Taï and Tiwai. As Chapman and colleagues (2004) recognized in guenon diets across sites in Eastern and Central Africa., I expect there to be dietary variation within the population of Diana monkeys. Finally, I compare Diana monkey diets to those of other guenons (Chapman et al. 2002) in order to expand our understanding of dietary adaptations within the genus Cercopithecus.

Chapter 2: Methods

Study Site

The Taï National Park is the largest remaining intact segment of the Upper

Guinea Forest, a forest belt which once covered West Africa from Ghana to Sierra Leone but has since been largely deforested across its former range (Martin 1991). The Taï

Forest, shown on the map in figure 1, is located in the southwest corner of Ivory Coast

(0°15’-6°07’N, 7°25’-7°54’W) and comprises 330,000 ha of protected forest with a

20,000 ha buffer zone surrounding the park’s boundary. Taï has been protected in some form since 1927, and has been listed as a UNESCO World Heritage Site since 1982

(McGraw and Zuberbühler 2007). However, it is still an area of conservation concern due to increasing pressure from the growing human population around the park and associated activities including illegal poaching, logging, forest clearing, and mining

(McGraw 2007b).

Though rainfall differs seasonally between two wet seasons and two dry seasons, the Taï Forest receives an average annual rainfall of 1893 millimeters/year (Anderson et al. 2005). Figure 2, from Anderson et al. 2005, shows fluctuations in monthly rainfall and mean maximum and minimum temperature at Taï during a period of comparable duration to this study, from July 1995-October 1999. To analyze seasonal differences in diet, I assigned seasons following Anderson et al. 2005: Dry Season 1 (November-March), Wet 7

Season 1 (April-June), Dry Season 2 (July-August), and Wet Season 2 (September-

October).

The Taï Forest is home to eight species of monkeys: four guenons (Cercopithecus diana, C. campbelli, C. petaurista, and C. nictitans), three colobines (Procolobus badius,

P. verus, and Colobus polykymos), and one mangabey (Cercocebus atys). The primate community in Taï also includes Pan troglodytes verus, the Western subspecies of the common chimpanzee, and several prosimians: Perodicticus potto and Galago demidoff

(McGraw, Cooke and Schultz 2006). Studies of the chimpanzee population by members of the Taï Chimpanzee Project are ongoing at several locations in the forest (Boesch and

Boesch-Ackermann 2000); studies of the cercopithecoid population are ongoing under the purview of the Taï Monkey Project. The presence of researchers at these sites offers protection for primates and duikers, with higher encounter rates for sensitive species in areas with ongoing research than outside of these areas (Cambell et al 2011).

Initiated by Ronald Noë and Bettie Sluijter, the Taï Monkey Project was founded in 1989 (McGraw and Zuberbühler 2007). Research was initiated on the red colobus and

Diana monkeys in 1991 in the main study grid. The study grid, 20 km from the nearest village and 25 km from the Liberian border, is located near the Institute d’Ecologie

Tropical field station and indicated in Figure 1 (McGraw and Zuberbühler 2007). The monkeys in this grid have been under nearly constant observation since the project’s inception. Three of the four Diana monkey groups that were studied have their home range in the main study grid of the Taï Monkey Project – Diana 1, Diana 2, and Diana 3.

The fourth group, Diana N, has its home range is about 5 km north of the main study grid.

Study Species

Diana monkeys are members of an extremely diverse tribe of monkeys, the

Cercopithecini, or guenons. Though they range from Mauritania to South Africa and occur in a staggering variety of habitats, the guenons are a relatively recent adaptive radiation of primates which have probably only been diversifying for the past million years (Butynski 2002). Like the other cercopithecinae, guenons are united by a number of adaptations for frugivory, including cheek pouches and bilophodont molars (Fleagle

1999). However, they can be distinguished from the papionins by their third lower molar, which is four-cusped and lacking a hypoconulid, and their diploid chromosome number which is always greater than 42 (Butynski 2002). Following the taxonomy in Butynski

(2002), the guenons comprise four genera, 23 species and 55 subspecies, which can also be divided into 10 superspecies or groups.

This study focuses on Cercopithecus diana diana, a member of the Diana superspecies which also includes C. d. roloway, a subspecies restricted to Eastern Cote d’Ivoire and Ghana (Curtin 2002). As shown in Figure 3, Diana monkeys are striking arboreal frugivores, conspicuous both in terms of coloration and their active, noisy, lifestyle (McGraw and Zuberbühler 2007, McGraw and Zuberbühler 2008). They are sexually dimorphic: males have a mean body weight of 5.2 kg, females 3.9 (Oates et al.

1990), though females have relatively larger canines and are less sexually dimorphic than many other guenons (Plavcan 1990). At Taï, Diana monkeys have an average group size

9 of 23.5 individuals, with one male, 11-13 females, and their offspring (Buzzard and

Eckardt 2007). As in most guenons, female Diana monkeys are philopatric, while males disperse from their natal groups.

Diana monkeys are almost always found in association with other monkeys; during the five years of this study Diana monkey groups were solitary during fewer than

5% of observations. This seems to be the result of targeted behavior by other monkey groups, particularly colobines (Oates and Whitesides 19990) perhaps due to the functionally distinct alarm call behavior Diana monkeys exhibit in response to leopards and crowned eagles (Zuberbühler 2007). Diana monkeys are central to the adaptive strategies of colobine monkeys at Taï and maintain regular associations with the other guenons in the forest as well (Buzzard 2006), suggesting that Cercopithecus diana is vital to the ecology of the Taï forest. Unfortunately, the 2008 IUCN Red List considers Diana monkeys Vulnerable, with a decreasing population, and our knowledge of this rare monkey remains limited.

Behavioral Sampling Methods

Data were collected between July 2004 and July 2009 by field assistants of the

Taï Monkey Project. This study focused on four groups of Diana monkeys: three contiguous groups (Diana 1, Diana 2, and Diana 3) in the main study grid of the Taï

Monkey Project, and one (Diana N) located about 5 kilometers north of the main study grid. Overall sampling effort and the sampling effort for each group is presented in Table

1, in Appendix B.

Instantaneous scan samples (Altmann 1974) were taken every thirty minutes on all visible individuals. Each scan recorded age and sex-class, forest height, and behavior.

Animals were not individually indentifiable; instead they were identified as Adult Female

(AF), Adult Male (AM), or Sub-adult (SX) based on visual cues. Where identification was not possible to age or sex-class, they were identified simply as X. Behavior was coded according to an ethogram, with the possible behaviors of Cling, Feed, Groom,

Locomote, Rest, and Social Play. If the individual was feeding, the observer noted the food part being eaten – fruit, leaf, insect, or other. Additionally, the observer noted specific attributes of the food (e.g. ripe fruit, young leaf, insect on leaf) and the species of the tree from which it came.

The height of the animal was recorded according to the categories in figure 4

(McGraw 1998). Homogeneity of forest height and composition was assumed, such that height categories are consistent across the forest. Forest height was scored from 0-4: ground level (0), shrubs and saplings below 5 meters (1), the understory (2), the lower canopy (3-), the upper canopy (3+), and the emergent layer (4).

Phenological Sampling Methods

Phenological data were collected approximately every two weeks from July 2005 to May 2010 on almost 300 trees from 59 species along a transect in the main study grid, with some gaps in transects. During these phenology transects, each tree was scored from

0-3 based on abundance of mature and young leaves, ripe and unripe fruit, and open and closed flowers. To account for uneven sampling effort across the study (both temporally and by number of trees per species), I created a weighted average phenological score for

11 each species by month, pooling the scores of individuals trees of each species and dividing by the number of trees included in that phonological transect. Consequently, this measure does not give an accurate picture of annual phenological variation at Taï.

However, when looking at monthly variation of Diana monkey diet, I followed a similar protocol by pooling monthly data from all four groups across the 5 years the study covered. Therefore, while neither measure gives a complete picture of annual variation, both measures allow me to generalize about the connections between monthly variation in fruit and leaf availability, and the relative importance of these as foods.

Statistical Methods

To test for differences in diet, I used SPSS and Minitab to run two-tailed

ANOVAs, and the Tukey-Kramer method to make multiple comparisons when appropriate. Alpha levels for all tests were set at 0.05. To test for variation in food consumption I used gross dietary categories (Fruit, Insects, Leaves, Other) and also tested for variation in consumption of the eight foods that, with insects, comprised 85% of the diet for all groups across the entire study.

I used ANOVA to test for interdemic dietary variation, comparing the diet of

Diana 1, Diana 2, and Diana 3 (the contiguous groups) to that of Diana N (the group approximately 5 km north) over the 5 years of this study. To compare our findings with results from previous studies that pooled data from multiple groups (Buzzard 2006, Oates and Whitesides 1990, Galat and Galat-Luong 1985, Curtin 2002), and to multiple guenon species (Chapman et al. 2002), feeding observations from each group were pooled to create a “meta-Diana” group. The pooled “meta-Diana” group was also used to test for

12 annual, seasonal, and monthly variation, as well as for variation in diet across different forest strata and different age- and sex-classes. This meta group provides an accurate summary of the diet of Diana monkeys at Taï over the study period because, as reported in Tables 2 and 3, there was no significant difference in consumption of any of the gross dietary categories. Of the eight most frequently consumed plant foods, only consumption of Oldfieldia africana differed significantly between Diana monkey groups, and that only varied between 1.53% and 5.61% of the diet.

Chapter 3: Results

Group Diet

The gross annual diet of each of the four study groups is reported in table 2 and figure 5. Fruit comprised at most 72.99% of the diet, and as little as 68.17%.

Consumption of insects showed slightly more variation, making up between 27.42% and

21.53% of the diet. Leaves made up between 3.90% and 5.22% of the diet. Other material, which included fungus, unidentified objects, seeds, and flowers, accounted for no more than 0.51% of the total diet, and as little as 0.18%. Over the five years of this study, the meta-Diana group diet was 70.36% fruit, 24.68% insects, 4.60% leavs, and

0.36% other material. An ANOVA showed no significant difference in the consumption of fruit (f=1.13, p=0.336), insects (f=1.70, p=0.168), leaves (f=1.70, p=0.168), or other material (f=1.70, p=0.255) in the diet of the four Diana monkey groups in this study.

Nine foods – insects and 8 parts of plants – comprise 84.05% of the total Diana monkey diet at Taï. These include seven ripe fruit species: Dialium aubrevillei (pictured in figure 6), Sacoglottis gabonensis (pictured in figure7), Scytopetalum tieghemii

(pictured in figure 8), Diospyros soubreana (pictured in figure 9), Diospyros mannii

(pictured in figure 10), Oldfieldia africana, and Parinari excelsa (pictured in figure 11).

It also includes one species of mature leaves, Craterispermum caudatum, which is pictured in figure 12. Group consumption of the eight most frequently eaten plant parts is 14 reported in Table 3 and Figure 13. For all four groups, Dialium aubrevillei and

Sacoglottis gabonensis are the two fruits most frequently consumed. While mean average consumption is greater for D. aubrevillei than S. gabonensis, D. aubrevillei is eaten less frequently by Diana 1 and Diana 2 than S. gabonensis. D. aubrevillei consumption ranges from 23.87% to 9.90% of the group diet; S. gabonensis from 20.60% to 5.39%. The other six plant parts each make up less than 6% of the mean diet, but actual group consumption ranges from 10.10% (Scytopetalum tieghemii, Diana 1) to 1.53% (Oldfieldia africana,

Diana 2). Craterispermum caudatum is the only leaf species of the eight most frequently consumed plant parts. Mean consumption is 4.42%, and only varies from 3.78% to

5.27%.

Despite variation in consumption by group, the ANOVA shows no significant difference in group consumption of Dialium aubrevillei (f=0.73, p=0.544), Sacoglottis gabonensis (f=2.45, p=0.066), Scytopetalum tiegehemii (f=1.77, p=0.166), Diospyros soubreana (f=0.83, p=0.490), Diospyros mannii (f=0.60, p=0.623), Craterispermum craudatum (f=0.92, p=0.432), or Parinari excelsa (f=1.45, p=0.239). However, consumption of Oldfieldia africana differed significantly between Diana 2 and Diana 1 and 3 (f=10.77, p<0.001).

Temporal Variability

Annual Dietary Variation

The annual diet was calculated for 2005-2008, years in which there were feeding observations taken in all months. These data are presented in Table 4 and figure 14. Fruit consumption was highest in 2005 (75.52%) and lowest in 2007 (62.32%); insect

15 consumption was lowest in 2005 (20.43%) and lowest in 2007 (32.71%). Leaf consumption varies from 2.81% in 2008 to 7.43% in 2006, and consumption of other material varies between 0.21% in 2008 to 0.57% in 2005. The ANOVA shows that annually, the Cercopithecus diana diet varies significantly in its proportion of fruit

(f=3.94, p=0.027), insects (f=11.00, p<0.001), and leaves (f=10.13, p<0.001), though not in its proportion of other material (f=0.22, p=0.881).

Table 5 and Figure 15 show the proportion in the annual diets of the eight plant parts most frequently consumed by Diana monkeys. Though there is variation in annual consumption of Dialium aubrevillei – from 6.11% in 2006 to 26.61% in 2007, annual consumption does not significantly differ (f=1.71, p=0.174). Sacoglottis gabonensis makes up between 7.36% (2007) and 25.46% (2006) of the annual diet; however consumption does not significantly differ inter-annually (f=1.45, p=0.666). Consumption of Scytopetalum tieghemii (f=1.69, p=0.200), Diospyros mannii (f=2.22, p=0.132) and

Craterispermum caudatum (f=2.15, p=0.065) also does not significantly differ inter- annually. However, annual consumption of Diospyros soubreana (f=3.08, p=0.048),

Oldfieldia africana (f=34.85, p<0.001), and Parinari excelsa (f=3.64,p=0.025) does differ significantly.

Seasonal Dietary Variation

Figure 16 shows the seasonal consumption of fruits, leaves, insects, and other material. Fruit consumption peaks in the first dry season and second wet season, between

July and October, between 74.69 and 74.88% of the diet. During the second dry season and first wet season, from November through June, fruit consumption decreases to

16 between 63.44 and 64.61% of the diet. Insect consumption follow the opposite pattern, peaking during the second wet season and first dry season between 28.22 and 28.15%, and decreasing during the first wet season and second dry season to 22.62 and 21.42% of the diet. Similarly, leaf consumption peaks during the second wet season and first dry season between 7.93% and 6.94%, and drops during the first wet season and second dry season between 2.37% and 3.19% of the diet. While the Cercopithecus diana diet (figure

3) varies significantly in consumption of leaves (f=15.80, p<0.001) between seasons, it does not vary significantly in fruit (f=1.79, p=0.909), insects (f=1.88, p=0.135), or other material (f=0.39, p=0.758).

Table 6 and Figure 17 show seasonal consumption of the eight most frequently consumed plant parts. Consumption of Sacoglottis gabonensis and Dialium aubrevillei peak in opposite seasons – Sacoglottis gabonensis in the first dry season and especially the second wet season, and Dialium aubrevillei in the second dry season and first wet season. Craterispermum caudatum makes up between 2.21 and 6.00% of the diet across all seasons. Consumption of Diospyros mannii (f=5.49, p=0.025), Diospyros soubreana

(f=15.03, p=0.002), Oldfieldia africana (f=26.65, p<0.001), and Sacoglottis gabonensis

(f=6.17, p=0.019) does differ significantly by season. However, consumption of

Craterispermum caudatum (f=2.10, p=0.183), Dialium aubrevillei (f=3.46, p=0.073),

Parinari excelsa (f=0.92, p-0.502), and Scytopetalum tieghemmii (f=0.79, p=0.568) does not significantly differ.

Monthly Diet

Monthly consumption of fruits, insects, leaves, and other material are presented in

Table 7 and Figure 18. Fruit consumption is highest in January (83.61%) and September

(79.03%), and at its lowest in April (53.39%) and December (54.79%). Insect consumption is at its highest in April (33.90%) and December (44.81%), and lowest in

January (14.87%) and September (17.49%). Leaf consumption is at its highest in April

(12.29%), and otherwise varies between 0.20% (December) and 7.60% (July). Other material never comprises greater than 0.79% of the monthly diet (September). Monthly, the Cercopithecus diana diet (figure 5) varies significantly in the consumption of fruit

(f=3.94, p<0.001), insects (f=2.05, p=0.026), and leaves (f=5.83, p<0.001). There is no significant difference in monthly dietary proportions of other material (f=1.17, p=0.310).

Figure 19 shows fruit consumption in 2008, as well as the mean monthly rainfall. Though it was not tested statistically, in 2008 rainfall was at its lowest level during January, the month with the highest fruit consumption, and at its highest during September, the month with the second highest fruit consumption. The relationship between rainfall and the proportion of fruit in the diet is not a straightforward one.

Table 8 and Figure 20 show monthly consumption of the eight most frequently consumed plant parts. Most striking are the patterns of consumption of Dialium aubrivellei and Sacoglottis gabonensis, which make up the bulk of the annual diet and may be the keystone species for Diana monkeys at Taï. Consumption of these two fruits peak at opposite times. Sacoglottis gabonensis makes up 35.20% of the diet in August,

69.65% in September, and 42.65% in November. Between January and June, Dialium aubrevillei comprises between 12.61 and 31.75% of the monthly diet. Other plants

18 comprise no greater than 24.9% of the monthly diet (Diospyros soubreana in January,

Scytopetalum tieghemii at 24.60% in November). Scytopetalum tieghemii (f=0.51, p=0.764) is the only fruit which did not show a significant difference in consumption during months it was eaten; however, it was only eaten between February and August.

Consumption of the other seven plant parts most frequently consumed differed significantly by month: Dialium aubrevillei (f=2.28, p=0.031), Sacoglottis aubrevillei

(f=9.86, p<0.001), Diospyros soubreana (f=2.59, p=0.024), Diospyros mannii (f=4.24,

[=0.009), Craterispermum craudata (f=2.18, p=0.019), Oldfieldia africana (21.75, p<0.001), and Parinari excelsa (f=5.27, p<0.001).

Figures 21 through 26 show relative monthly consumption of seven of the eight most frequently consumed plant parts, and the average monthly phenological abundances of ripe fruit and unripe fruit, or mature and young leaves. The relationships between consumption and abundance were not statistically tested, but are represented graphically.

Figure 21 shows the relationship between Dialium aubrevillei and Sacoglottis gabonensis consumption and phenological availability; it appears that consumption of Sacoglottis gabonensis fruit peaks when phenological abundance of ripe fruit peaks, and Dialium aubrevillei consumption peaks after fruit availability begins to decline. Scytopetalum tieghemii and Oldfieldia africana, Figures 22 and 23, seem to have patterns of phenological abundance and consumption like that of Sacoglottis gabonensis, where consumption and abundance peak at approximately the same time. Figure 24 shows that mature leaves of Craterispermum caudatum are available at the same level year round, though consumption varies significantly from month to month. Figure 25 (Parinari

19 excelsa) and 26 (Diospyrum soubreana) show trees with more complex relationships between consumption and abundance.

Dietary Variation Across Forest Strata

Figure 27 and Table 9 shows the relationship between Diana monkey diets and forest height. Though fruit is the most frequently consumed food at all levels of the forest, between the understory and the emergent layer, insects are the next most frequently consumed food item (between 15.75 % and 38.4%). In the shrub and sapling layer, leaves are the second most frequently consumed food (36.62%). Fruit is the only food consumed at ground level. The ANOVA shows that there are significant differences in the frequency of consumption of different foods at ground level (f=41.19, p<0.001), the sapling layer (f=28.77, p<0.001), the understory (f=23.16, p<0.001), the lower canopy

(f=67.46, p<0.001) the upper canopy (f=66.76, p<0.001), and the emergent layer

(f=13.11, p<0.001).

Figure 28 and Table 10 show consumption of the eight most frequently consumed plant parts in each forest strata. Dialium aubrevillei consumption is most frequent in the lower and upper canopy, where this fruit makes up 22.98% and 26.75% of the food consumed in each level. Sacoglottis gabonensis is eaten in all strata but the emergent layer. 75.78% of food consumed on the ground is Sacoglottis gabonensis; Parinari excelsa makes up the remaining quarter. Sacoglottis gabonensis is also often consumed in the sapling layer, comprising 37.90% of the food eaten there. Another 35.58% of the foods consumed in this stratum are mature leaves of Craterispermum caudatum. Parinari excelsa and Oldfieldia africana are the plant foods most frequently consumed in the

20 emergent layer. Diospyros mannii (22.67%) and Diospyros soubreana (22.83%) are both important components of the diet eaten in the understory. The ANOVA shows significant differences between the frequency of species eaten at ground level (f=3.78, p<0.001), the sapling and shrub layer (f=3.07, p=0.004), the understory (f=2.80, p=0.008), the lower canopy (f=2.65, p=0.012), the upper canopy (f=3.06, p=0.004), and the emergent layer

(f=3.73, p=0.001).

Age- and Sex-ClassVariation

Figure 29 and Table 11 show the consumption of fruit, insects, and leaves by adult males, adult females, and subadults. Subadults eat the highest proportion of fruit

(68.55%), followed by adult males (66.79%), and adult females the lowest (61.60%).

Adult females have the highest insect consumption (31.82%), followed by adult males

(30.09%) and subadults (24.17%). Subadults eat the highest proportion of leaves (7.28%), followed by adult females (6.58%) and adult males (3.11 %). Adult females, adult males, and subadults do not eat significantly different proportions of fruit (f=0.19, p=0.828) or insects (f=1.24, p=0.296). However, subadults eat a significantly greater proportion of leaves than adult males (f=4.04, p=0.022).

Figure 30 and Table 12 show the consumption of the eight most frequently consumed plant parts by adult females, adult males, and subadults. Sacoglottis gabonensis is most frequently consumed by all three age- and sex-classes, comprising

11.64% of the adult female diet, 15.66% of the adult male diet, and 14.48% of the subadult diet. Dialium aubrevillei is the next most frequently consumed food, comprising between 10.02 and 10.77% of the diet of each age- and sex-class. There is no significant

21 difference in the consumption of any of the eight most important plant foods (Figure 12):

Dialium aubrevillei (f=0.16, p=0.852), Sacoglottis gabonensis (f=0.48, p=0.624),

Scyopetalum tieghemii (f=0.52, p=0.600), Diospyros soubreana (f=0.27, p=0.768),

Diospyros mannii (f=1.93, p=0.154), Craterispermum caudatum (f=0.92, p=0.404),

Oldfieldia africana (f=2.52, p=0.093), or Parinari excelsa (f=2.95, p=0.066).

Interdemic Comparisons

Figure 31 and Table 13show the consumption of fruit, insects, leaves, and other material by the three contiguous groups (combined consumption of Diana 1, Diana 2, and

Diana 3) and the northern group (Diana N). The overall diet of the contiguous groups is

70.68% fruit, 24.44% insects, 4.47% leaves, and 0.40% other material. 69.02% of the northern group’s diet is fruit, 25.65% insects, 5.15% leaves, and 0.18% other material.

There is no significant difference in consumption of fruit (f=0.36, p=0.612), insects

(f=0.13, p=0.757), leaves (f=0.75, p=0.477), or other material (f=2.25, p=0.272).

Interdemic consumption of the eight most frequently consumed plant parts is shown in Figure 32 and Table 14. 23.97% of the northern group’s diet is Dialium aubrevillei as opposed to only 14.46% of the contiguous groups’ total diet. Sacoglottis gabonensis, meanwhile, is the most frequently consumed fruit by the contiguous groups

(17.71%) but only 5.39% of the northern group. Despite this interdemic variation, there is not a significant difference between consumption of Dialium aubrevillei (f=4.15, p=0.178) Sacoglottis gabonensis (f=5.82, p=0.137), Scytopetalum tieghemii (f=0.76, p=0.476), Diospyros soubreana (f=5.29, p=0.148), Diospyros mannii (3=0.06, p=0.825),

Craterispermum caudatum (f=0.36, p=0.610), Oldfieldia africana (f=0.06, p=0.833), and

Parinari excelsa (f=0.05, p=0.841).

Interpopulation Comparisons

Figure 33 and Table 15 compare the diet of the meta-Diana group from this study to previous studies of Cercopithecus diana diana (Galat and Galat-Luong 1978, Oates and Whitesides 1990, Buzzard 2006) and Cercopithecus diana roloway (Curtin 2002).

Diana monkeys from this study have the highest rate of fruit consumption of all populations, 70.43%, except for Diana monkeys at Taï in the 1970s (Galat and Galat-

Luong 1978). They are eating only slightly fewer insects (24.66%) than C. diana diana at

Tiwai Island from 1982-1984 (27.65%, Oates and Whitesides 1990) and C. diana roloway at Bia National Park in 1976 and 1977 (33.8%, Curtin 2002). They are eating the lowest proportion of leaves and other material of any population – in particular, they are eating many fewer seeds and flowers than Diana monkeys at Bia National Park (38.8%) and Tiwai Island (22.0%).

Interspecies Comparisons

Figure 34 and Table 16 provide a broader context for the reported diet of

Cercopithecus diana from this study. Cercopithecus diana eats a higher proportion of fruit and insects than any of the guenons whose diet are reported by Chapman and colleagues (2004). Cercopithecus cephus eats nearly as much fruit (67.17%) and insects

(17.11%) but supplement their diet with more leaves (6.76%), and seeds and flowers

(8.96%). While insects also comprise a large proportion of the Cercopithecus ascanius diet (22.04%), their diet is much richer in leaves (23.32%) and other material (14.69%)

23 than fruit (39.94%). Diana monkeys eat many fewer leaves than Cercopithecus ascanius,

Cercopithecus mitis (20.36%), and Cercopithecus nictitans (12.90%), and have the lowest rate of consumption of other material of any of these guenons. In this context,

Diana monkeys are frugivores supplementing their diets with insects; most of the other guenons are less reliant on fruit and insects and eat a higher proportion of leaves, flowers, and seeds.

Chapter 4: Discussion and Conclusions

Group Variability

I first tested the null hypothesis that Diana monkey groups at Taï show no intergroup dietary variation, predicting that I would find significant variation between group diets. Contrary to my expectations, the diets of the four Diana monkey groups at

Taï did not significantly differ in their consumption of fruit, insects, leaves, or other material. Over the five years of this study, the meta-Diana monkey group’s diet was

70.36% fruit, 24.68% insects, 4.60% leaves, and 0.36% other material.

85% of the diet is comprised of insects and the parts of eight plants, listed in

Table 3. Ripe fruit of Oldfieldia africana was the only dietary component that varied significantly between groups. However, lack of statistical significance may obscure biological significance. Sacoglottis gabonensis, for example, is the second most frequently consumed plant part for the meta-Diana group, 15.39% of the total diet.

Consumption does vary between the groups: Sacoglottis gabonensis is 20.60% of the total diet of Diana 1, 19.92% of the Diana 2 diet, 12.62% of the Diana 3 diet, and just

5.39% of the diet of Diana N. Because the groups exhibit a range of rates of consumption, the difference between all the groups may not be statistically significant,

25 but the disparity in Sacoglottis gabonensis consumption may have real nutritional consequences for these groups.

Despite this variation in consumption of particular species, there is a striking overall similarity in Diana monkey diets, particularly in proportions of fruit, insects, leaves, and other material in the diet. This is interesting given that Diana monkeys have a demonstrably high level of inter-group aggression, a trait which is often used to infer competition for food resources (Isbell 1991). According to Wrangham’s model (1980) and later expansions of the model that include predation and resource distribution (Van

Schaik 1989, Isbell 1991, Sterck et al. 1997, Isbell and Young 2002), females are driven to aggression in order to protect access to high quality, patchy resources like fruit.

Buzzard and Eckardt (2007) spent 95 days observing Diana monkeys at Taï and observed one intergroup encounter about every three days; 35% of those encounters were aggressive and tended to be related to access to a particular feeding tree. Buzzard and

Eckardt also measured the home range of Diana 1 (59.3 hectares) and Diana 2 (58.5 hectares) and found an overlap between 65% and 67% of the total home range. If each pair of contiguous groups have such high rates of home range overlap, monopolizing access to a particular fruiting tree through direct or scramble competition may be worth the immediate energetic output and risk of injury for the immediate nutritional benefits it would confer. Risks from fighting are real for Diana monkeys as evidenced by the intraspecific killing observed by McGraw and colleagues (McGraw et al. 2002). Feeding observations as they were pooled here are likely at too coarse a scale to detect the effects of day-to-day intergroup dietary competition.

It may be possible to identify the effects of group dominance through other metrics. If a more dominant group is monopolizing higher-quality forest patches, they would need to expend less energy accessing preferred resources. Subordinate groups may have to travel farther and spend more time feeding to maintain the necessary level of fruit in their diet, working harder to meet their nutritional needs. They may need to utilize larger home ranges in order to travel to a greater number of lower quality patches, and they may be restricted to generally lower quality forest. Additionally, activity budgets of nutritionally-stressed animals tend to be shifted towards more time spent traveling and foraging, and feeding than their counterparts in higher quality habitat (Menon and Poirier

1996, Li and Rogers 2004). Drawing a distinction between time spent feeding and time spent foraging in further study of adjacent group diets would provide a test of the hypothesis that dominance and subordinance are reflected in effort to maintain their diet, rather than in the components of their diet. Additionally, more accurate measures of fruit abundance and forest quality would help clarify the relationship between diet, food availability, and inter-group aggression.

Temporal Variability

I tested the null hypothesis that Diana monkey diets at Taï do not vary in their composition annually, seasonally, or monthly, predicting that I would find significant dietary variation at each temporal level.

Annual Dietary Variation

As I predicted, for the four years in which data were collected during all months, annual consumption of fruits, leaves, and insects differed significantly. Fruit was between 27

75.5% and 62.3% of the annual diet, insects between 32.7% and 20.4%, and leaves between 7.43% and 2.81%. These variations are likely due to inter-annual variation in fruit availability. At Taï, most trees fruit, flower, and leaf-flush on an annual cycle; however there are deviations from this cyclical pattern in response to fluctuations in temperature or rainfall (Anderson et al. 2005).

Annual consumption of Dialium aubrevillei and Sacoglottis gabonensis did not differ significantly, and together these fruit make up about a third of the annual diet.

However Dialium aubrevillei made up between 6.1% and 26.6% of the annual diet and

Sacoglottis gabonensis consumption exhibited a similar fluctuation in contribution to the annual diet, varying between 7.36% and 25.46%. Interestingly, the year of highest

Dialium aubrevillei consumption (2006) was the year of lowest Sacoglottis gabonensis consumption, and vice versa. While my phenological analysis did not identify whether there was low availability of either of these fruits in 2006 and 2007, it appears that consumption of Dialium aubrevillei is highest when Sacoglottis gabonensis consumption is lowest, and vice versa.

Seasonal Dietary Variation

As I predicted, Diana monkey diets exhibited significant seasonal variation in diet. Fruit consumption peaks during the first dry season and second wet season (between

July and October) when the diet is about 75% fruit. Fruit drops to about 64% of the diet during the second dry season and first wet season (from November to June), although this is opposite the pattern of fruit abundance at Taï, shown in Figure 35 (Anderson et al.

2005). Insect consumption follows the opposite pattern, about 28% of the diet during the

28 first wet season and second dry season and between 21% and 22% during the second wet season and first dry season. Leaf consumption follows the same pattern as insect consumption: intake is between 7-8% in those seasons with lowest fruit consumption and between 2-3% in seasons with high fruit consumption. This suggests that Diana monkeys supplement their diet with leaves and particularly insects during those periods when fruit is scarce.

Monthly Dietary Variation

Monthly fruit consumption exhibits two peaks. It is highest in January (83.6%), which is right during peak fruit abundance, and September (79.0%), the month in which phonological productivity peaks for Sacoglottis gabonensis. Dialium aubrevillei and

Diospyros soubreana are each about 25% of the diet during January, and January is a month in which both of these trees experiences peaks in ripe fruit. The total diet in

September is about 70% Sacoglottis gabonensis. Though not statistically tested, it looks like consumption of Sacoglottis gabonensis is focused on those months in which it has the greatest phonological availability. Figure 20 shows the relationship between phenology and consumption of Dialium aubrevillei and Sacoglottis gabonensis. Again, though not statistically tested, consumption of both fruits peak in conjunction with peaks in fruit availability. Months with the lowest consumption of fruit, April (53.4%) and

December (54.8%), are the months with the highest rates of insect consumption (33.9% and 44.8% respectively). In April, 12.3% of the diet is also leaf material. Again, Diana monkeys are supplementing their diet with insects and leaves when they are not eating lots of fruit.

Diana Monkeys and Fallback Foods

Diana monkeys provide a useful test case to evaluate the utility of fallback foods as an explanatory concept. Fallback foods are defined as resources of low preference used seasonally to supplement diet at times when preferred foods have low abundance

(Marshall and Wrangham 2007). They are generally identified based on mechanical properties (Lambert et al.2004), relative abundance, and consumption in relation to more preferred foods. Specifically, fallback foods are implicated in the development of thick dental enamel in grey-cheeked mangabeys (Lambert et al. 2004), the sacculated gut of colobines (Marshall and Wrangham 2007), and lowered levels of aggression in bonobo populations as opposed to chimpanzee populations (Wrangham 1986, White 1998), and are touted for their potential explanatory power (Constantino and Wright 2009, Marshall et al. 2009).

The two fruits which are most frequently eaten by Cercopithecus diana at Taï are

Dialium aubrevillei and Sacoglottis gabonensis. Dialium aubrevillei, shown in figure 6, may fulfill the mechanical requirements of a fallback food (Lambert et al. 2004). They are small pellet-like fruits without much pulp, and require some degree of mechanical processing in order to be eaten. Sacoglotis gabonensis, shown in figure 7 and being eaten by a Diana monkey in figure 3, are more energy-rich and easier to consume by virtue of their pulpy flesh. Looking purely at mechanical properties, Dialium aubrivellei could be identified as a fallback food. However, Dialium aubrivellei is the most frequently consumed fruit during the peak period of fruit abundance, between November and June, despite the abundance of other fruits which may be easier to eat and in more nutrient-rich

30 forms. In contrast, Sacoglottis gabonensis is the most frequently consumed fruit during the months where it is available, months in which overall fruit abundance is lowest – times when primates are assumed to be utilizing fallback foods.

The fallback food concept seems to be an oversimplification of primate dietary complexity, and is a concept which does not need to be relied upon to explain patterns of guenon dietary variation. Classifying foods as fallback or preferred foods imposes a false dichotomy on primate diets which are flexible and variable at a number of levels.

Overreliance on fallback foods as an explanatory mechanism for primate diets and morphology may obscure other relationships between ecology, morphology, and sociality

(Marshall et al. 2009), particularly considering the vast capacity for interspecific dietary variation exhibited across primate taxa.

Dietary Variation Between Forest Strata

I tested the null hypothesis that Diana monkeys eat the same foods across all forest strata, predicting that Diana monkeys would eat different things in each forest strata. As I predicted, Diana monkeys ate different proportions of different foods in each level of the forest. Fruit is the most frequently consumed food at all forest levels. 38.9-

15.75% of what Diana monkeys ate between the understory and the emergent layer was insect material, and leaves were 36.6% of the food eaten in the sapling layer. Fruit of

Sacoglottis gabonensis and Parinari excelsa are the only food items consumed on the ground. Figure 34 summarizes Diana monkey behavior across forest strata; at ground level feeding is the most frequently performed behavior. Though Sacoglottis gabonensis is regularly consumed in the canopy, Diana monkeys regularly descend to the ground to

31 eat its fallen fruit. McGraw and Zuberbühler (2008) hypothesize that predation risk may be greater lower in the forest than in the canopy, due to the cryptic behavior of monkeys frequently found in the understory (for example, olive colobines) compared to conspicuous monkeys specializing in the canopy (for example, red colobus and Diana monkeys). If this is the case, Diana monkeys are willing to increase their risk of predation to access Sacoglottis gabonensis fruit on the forest floor.

Dietary Variation Between Age- and Sex-Classes

I next tested the null hypothesis that Diana monkeys of different age- and sex- classes have the same diets, predicting that diets will differ across age- and sex-class.

Contrary to my expectations, the proportion of fruit and insects in the diet of adult male, adult female, and subadult Diana monkeys does not significantly differ. However, adult females and subadults ate a higher proportion of leaves than adult males; this difference was statistically significant when subadults and adult males were compared. There is no significant difference in the proportions of any of the eight most frequently consumed plants parts in the diets of adult males, adult females, or subadults.

This differs from the pattern observed in C. mitis and C. ascanius (Cords 1986a), in which individuals of different age- and sex-classes have diets more similar to those of other members of their age- and sex-class outside of their species than to those of conspecifics of different age- or sex-classes. One possible explanation for this pattern is that the high rate of polyspecific associations in Diana monkeys constrains their diets such that all Diana monkeys are eating essentially the same things. C. mitis and C. ascanius are found in polyspecific associations at a much lower rate than C. diana (Cords

1986b, Buzzard 2006). However, since Diana monkeys dominate the other monkeys they associate with, this is not a likely explanation (McGraw and Zuberbühler 2007). A confounding factor in this analysis is that because this study did not identify all individuals to age- and sex-class, only a small subset of observations was included. This analysis included 12,548 observations, only 19% of the total sampling effort.

Interdemic Dietary Variation

Next, I tested the null hypothesis that Diana monkey groups at Taï which are part of different demes have diets that do not vary, predicting that the three contiguous groups would have diets which were more similar than the northern group. In fact, while the northern group ate a diet divergent from the pooled diet of the contiguous group, there was a range of consumption within the three contiguous groups such that there was no significant difference in consumption of fruit, leaves, insects, or any of the eight most frequently consumed plant parts between the northern group and the groups in the study grid. The 5 kilometers separating Diana N from Diana 1, 2, and 3 may not be a great enough distance to adequately differentiate between demes; Butynski (1990) found interdemic variation between populations separated by 12 kilometers.

Interpopulational Dietary Variation

The diet reported for Cercopithecus diana diana in this study, compiled from study of four groups over five years, differs from diets reported from previous studies of

C. d. diana at Taï (Galat and Galat-Luong 1978, Buzzard 2006) and Tiwai Island (Oates and Whitesides 1990), and C. d. roloway at Bia National Park (Curtin 2002). All studies of C.d. diana ate a higher proportion of fruit than C. d. roloway (20.9%); however the

33 diet of C. d. diana at Tiwai Island was only 26.52% fruit. Insects and other material comprised a greater proportion of the diet at both of these sites than at Taï in any study

The proportion of fruit in the diet for this study (70.4%) was greater than reported at Taï from 2000-2001 (59%), but slightly less than the study from the mid-1970s (76.3%).

Inter-annual differences in the Diana monkey diet at Taï may be the result of variation in rainfall and phenology, leading to differences in fruit abundance. At Tiwai Island, the relative diversity of the Diana monkey diet may be a consequence of the a more marginal island habitat with a less diverse forest (May and Stumpf 2000).

Characterizations of Cercopithecus diana as an arboreal frugivore that supplements its diet primarily with insects and mature leaves are not changed by the addition of these 5 years of feeding data, though updated studies of C. d. diana outside of

Taï and C. d. roloway may change our characterization of the typical Diana monkey. The

Diana monkeys at Tiwai Island have not had dietary studies since Oates and Whitesides’ study between 1982 and 1984, and the highly endangered C. d. roloway has not received any attention since the 1970s. It is possible, and indeed likely, that inter-annual variation in the diets of populations at these sites would add to our understanding of dietary flexibility in Cercopithecus diana. Though Cercopithecus diana is among the most- recognized West African guenons, it is remarkably poorly understood compared to its better-known East and Central African counterparts.

Interspecies Dietary Variation

Finally, I compared Diana monkey diets found here with those reported from studies of other guenons across Africa by Chapman and colleagues (2002). Though this

34 was not statistically tested, I expected to see variation between Cercopithecus diana and other cercopithecines. Indeed, Cercopithecus diana is the most frugivorous of all the guenons studied, and eats the highest proportion of insects, and the lowest proportion of leaf and other material of all these species. There seems to be a similar capacity for interpopulation variation across the guenons, though the guenons included by Chapman and colleagues are known from more sites.

Directions For Further Study

Further study of Diana monkey variability could take a number of different directions. Diana monkeys at Taï are almost always involved in polyspecific associations

(Buzzard 2006), and the possible confounding effects on diet of association with the other guenons, with large-bodied colobines, and with terrestrial mangabeys demand further attention. A more accurate assessment of forest homogeneity and patterns of resource distribution across Taï would add explanatory power to studies of inter-group variation and the effects of seasonality on diets.

It would also be helpful to analyze the chemical and mechanical properties of the eight foods most frequently consumed to evaluate nutritional requirements and identify physiological adaptations. Since Diana monkeys at Taï eat a fairly large proportion of mature leaves each month, analyzing the leaves of Craterispermum caudatum could uncover further nutritional and dental adaptations of Diana monkeys. Patterns of insect consumption remain a relatively poorly known phenomena for species which are supplementing their diets with insects. Are Diana monkeys foraging opportunistically on

35 insects as they travel and forage for other foods, or are certain insects targeted for consumption?

Finally, further study into the context of inter-group aggression would clarify primate grouping patterns and the observed high rates of inter-group aggression in

Cercopithecus diana. One way this could be achieved is by measuring stress through the activity budgets and cortisol levels of different groups to understand how much effort groups put into maintaining dietary thresholds. This could be correlated with reproductive output, parasite load, and other measures of health and productivity to see the consequences of maintaining both high levels of inter-group aggression and extremely high rates of frugivory.

Conclusions

1. The proportion of fruit, leaves, insects, and other material in Diana monkey diets

does not vary significantly between groups.

2. Diana monkeys vary temporally: there is significant inter-annual variation in the

proportion of fruit, leaves, and insects in Diana monkey diets and significant

monthly variation in the proportion of fruit, leaves, and insects in Diana monkey

diets.

3. Fruit is the most frequently consumed food in all forest strata. Leaf consumption

is limited to the shrub and sapling layer, while insect consumption occurs in the

understory, canopy, and emergent layer.

4. Adult females, adult males, and subadults do not eat different proportions of fruit

or insects. However, subadults eat significantly more leaves than adult males do. 36

5. The diet of Cercopithecus diana diana in this study was exceptionally frugivorous

and more reliant on insect material than the diet of conspecifics in other

populations, or other cercopithecines. They ate fewer leaves, seeds, and flowers

than any other Diana monkey population or cercopithecine species considered.

References

Altmann J. 1974. Observational study of behavior: sampling methods. Behaviour 49 (3/4): 227-267.

Anderson DP, Nordheim EV, Moermond TC, Gone Bi ZB, and Boesch C.2005. Factors influencing tree phenology in Taï National Park, Côte d’Ivoire. Biotropica 37(4): 631-640.

Boesch C and Boesch-Ackermann H. 2000. The Chimpanzees of the Taï Forest. Oxford: Oxford University Press.

Butynski TM. 1990. Comparative ecology of blue monkeys (Cercopithecus mitis) in high and low density subpopulations. Ecological monographs 60: 1-26.

Butynski TM. 2002. The guenons: an overview of diversity and taxonomy. In: The Guenons: Diversity and Adaptation in African Monkeys ed. M. E. Glenn and M. Cords. New York: Kluwer Academic/Plenum Publishers. 3-13.

Buzzard PJ. 2006. Ecological partitioning of Cercopithecus campbelli, C. petaurista, and C. diana in the Taï Forest. International Journal of Primatology 27(2): 529-558.

Buzzard PJ and Eckardt W. 2007. The social system of the guenons. In: Monkeys of the Taï Forest: An African Primate Community, ed. W. S. McGraw and K. Zuberbühler. New York: Cambridge University Press. 51-71.

Campbell G, Kuehl H, Diarrassouba A, N’Goran PK, and Boesch C. 2011. Long-term research sites as refugia for threatened and over-harvested species. Biology Letters published online March 2011.

Chapman CA and Chapman LJ. 1990. Dietary variability in primate populations. Primates 31(1):121-128.

Chapman CA and Chapman LJ. 1999. Implications of small scale variation in ecological conditions for the diet and density of red colobus monkeys. Primates 40(1): 215- 231.

Chapman CA, Chapman LJ, Cords M, Mwangi Gathua J, Gautier-Hion A, Lambert JE, Rode K, Tutin CEG, and White LJT. 2002. Variation in the diets of Cercopithecus species: differences within forests, among forests, and across species. In: The Guenons: Diversity and Adaptation in African Monkeys ed. M. E. Glenn and M. Cords. New York: Kluwer Academic/Plenum Publishers. 325-350.

Chapman CA and Fedigan LM. 1990. Dietary differences between neighboring Cebus capucinus groups: local traditions, food availability, or responses to food profitability? Folia primatologica 54: 177-186.

Clutton-Brock TH. 1977. Some aspects of intraspecific variation in feeding and ranging behaviour in primates. In: Primate Ecology, ed. TH. Clutton-Brock. New York: Academic Press. 539-556.

Constantino PJ and Wright BW. 2009. The importance of fallback foods in primate ecology and evolution. American Journal of Physical Anthropology 140: 599- 602.

Cords M. 1986a. Interspecific and intraspecific variation in diet of two forest guenons, Cercopithecus ascanius and C. mitis. Journal of Animal Ecology 55: 911-827.

Cords M. 1986b. Mixed-species association of East African guenons: general patterns or specific examples? American Journal of Primatology 21: 101-114.

Curin SH. 2004. Diet of the Roloway Monkey, Cercopithecus diana roloway, in Bia National Park, Ghana. In: The Guenons: Diversity and Adaptation in African Monkeys ed. M. E. Glenn and M. Cords. New York: Kluwer Academic/Plenum Publishers. 351-371.

Fleagle J. 1999. Primate Adaptation and Evolution. Academic Press 1999.

Galat G and Galat-Luong A. 1985. La communaute de primates diurnes de la foret de Tai, Côte d’Ivoire. Terre Vie 40:3-32.

Gautier Hion A. 1980. Seasonal variations of diet related to species and sex in a community of Cercopithecus monkeys. The Journal of Animal Ecology 49: 237- 269.

Harris TR and Chapman CA. 2007. Variation in diet and ranging of black and white colobus monkeys in Kibale National Park, Uganda. Primates 48: 208-221.

Hawthorne W and Gyakari N. 2006. Photoguide for the forest trees of Ghana: a tree- spotter's field guide for identifying the largest trees. Oxford: Oxford Forestry Institute. 39

Hawthorne W and Jongkind C. 2006. Woody plants of western African forests: a guide to the forest trees, shrubs, and lianes from Senegal to Ghana.Richmond: Royal Botanica Gardens, Kew.

Hill CM. 1994. The role of female Diana monkeys, Cercopithecus diana, in territorial defense. Animal Behavior 47: 425-431.

Isbell LA. 1991. Contest and scramble competition: patterns of female aggression and ranging behavior among primates. Behavioral Ecology 2:143-155.

Isbell LA and Young TP. 2002. Ecological models of female social relationships in primates: similarities, disparities, and some directions for future clarity. Behaviour 139(2/3): 177-202.

Lambert JE. 2002. Resource switching and species coexistence in guenons: a community analysis of dietary flexibility. In: The Guenons: Diversity and Adaptation in African Monkeys ed. M. E. Glenn and M. Cords. New York: Kluwer Academic/Plenum Publishers. 309-324.

Lambert JE, Chapman CA, Wrangham RW, Conklin-Brittain NL. 2004. Hardness of cercopithecine foods: implications for the critical function of enamel thickness in exploiting fallback foods. American Journal of Physical Anthropology 125 (4): 363-368.

Leite YLR, Costa LP, and Stallings JR. 1996. Diet and vertical space use of three sympatric opossums in a Brazilian Atlantic forest reserve. Journal of Tropical Ecology 12: 435-440.

Li Z and Rogers R. 2004. Habitat quality and activity budgets of white-headed langurs in Fusui, China. International Journal of Primatology 25(1): 41-54.

Marshall AJ, Boyko CM, Feilen KL, Boyko RH, and Leighton M. 2009. Defining fallback foods and assessing their importance in primate ecology and evolution. American Journal of Physical Anthropology 140(4): 603-614.

Marshall AJ and Wrangham RW. 2007. Evolutionary consequences of fallback foods. International Journal of Primatology 28 (6): 1210-1236.

Martin C. 1991. The Rainforests of West Africa: Ecology, Threats, Conservation. Basel: Birkhäuser.

May RM and Stumpf MPH. 2000. Species-area relations in tropical forests. Science 490 (5499): 2084-2086. 40

McGraw WS. 1998. Comparative locomotion and habitat use of six monkeys in the Tai Forest, Ivory Coast. American Journal of Physical Anthropology 105: 493-510. McGraw WS and Bshary R. 2002. Association of terrestrial mangabeys (Cercocebus atys) with arboreal monkeys: experimental evidence for the effects of reduced ground predator pressure on habitat use. International Journal of Primatology 23(2): 311-325. McGraw WS. 2007a . Positional behavior and habitat use of Taï Forest monkeys. In: Monkeys of the Taï Forest: An African Primate Community, ed. W. S. McGraw and K. Zuberbühler. New York: Cambridge University Press. 223-253. McGraw WS. 2007b. Vulnerability and conservation of the Taï monkey fauna. In: Monkeys of the Taï Forest: An African Primate Community, ed. W. S. McGraw and K. Zuberbühler. New York: Cambridge University Press. 290-316.

McGraw WS, Cooke C, and Schultz S. 2006. Primate remains from African Crowned Eagle (Stephanoaetus coronatus) nests in Ivory Coast’s Tai Forest: Implications for primate predation and early hominid taphonomy in South Africa.

McGraw WS, Plavcan JM, and Adachi-Kanazawa K. 2002. Female Cercopithecus diana employ canine teeth to kill another adult female C. diana. International Journal of Primatology 23(6): 1301-1308.

McGraw WS and Zuberbühler K. 2007. The Monkeys of the Taï Forest: an introduction. In: Monkeys of the Taï Forest: An African Primate Community, ed. W. S. McGraw and K. Zuberbühler. New York: Cambridge University Press. 1-48.

McGraw WS and Zuberbühler K. 2008. Socioecology, predation, and cognition in a community of West African Monkeys. Evolutionary Anthropology 17: 254-266.

Menon S and Poirier FE. 1996. Lion-tailed macaques (Macaca silenus) in a disturbed forest fragment: activity patterns and time budget. International Journal of Primatology 17(6): 969-985.

Oates JF, Whitesides GH, Davies AG, Waterman OG, Green SM, Dasilva GL, and Mole S. 1990. Determinants of variation in tropical forest primate biomass: new evidence from West Africa. Ecology 71(1): 328-343.

Oates JF and Whitesides P. 1990. Associations between olive colobus (Procolobus verus), Diana guenons (Cercopithecus diana) and other forest monkeys in Sierra Leone. American Journal of Primatology 21: 129-146.

Plavcan JM. 1990. Sexual dimorphism in the dentition of extant anthropoid primates. Ph.D dissertation. http://proxy.lib.ohio- state.edu/login?url=http://search.proquest.com/proxy.lib.ohio- state.edu/docvies/303855825?accountid=9783

Struhsaker TT. 1967. Ecology of the vervet monkeys (Cercopithecus aethiops) in the Masai-Amboseli Game Reserve, Kenya. Ecology 48(6):891-904.

Thomas CD, Cameron A, Green RE, Bakkanes M, Beaumont LJ, Collingham YC, Erasmus BFN, Ferreira de Siquara M, Grainger A, Hannah L, Hughes L, Huntley B, van Jaarsvald AS, Midgley GF, Miles L, Ortega-Huerta MA, Peterson AT, Phillips OL, and Williams SE. 2004. Extinction risk from climate change. Nature 427: 145-148.

Tutin CEG and Fernandez M. 1993. Composition of the diet of chimpanzees and comparisons with that of sympatric lowland gorillas in the Lopé Reserve, Gabon. American Journal of Primatology 30(3): 195-211.

White F. 1998 Seasonality and socioecology: the importance of variation in fruit abundance to bonobo sociality. International Journal of Primatology 19: 1013– 1027.

Wrangham RW. 1980. An ecological model of female-bonded primate groups. Behaviour 75(3/4):262-300.

Wrangham RW. 1986. Ecology and social relationships in two species of chimpanzee. In D. I. Rubenstein and RW Wrangham, eds. Ecology and social evolution: birds and mammals. Princeton: Princeton University Press. 352-378.

Zelazowski P, Malhi Y, Huntingford C, Sitch S, and Fisher JB. 2011. Changes in the potential distribution of tropical forests on a warmer planet. Philosophical transactions of the Royal Society of Mathematical, Physical, and Engineering Sciences 369 (1934):137-160.

Zuberbühler K. 2007. Monkey Alarm Calls. In: Monkeys of the Taï Forest: An African Primate Community, ed. W. S. McGraw and K. Zuberbühler. New York: Cambridge University Press. 194-220.

Appendix A: Figures

Figure 1. The location of the Taï Forest.

Figure 2. Mean monthly rainfall and average minimum and maximum temperatures in the Taï Forest (Anderson et al. 2005).

Figure 3. Cercopithecus diana eating Sacoglottis gabonensis fruit at the Taï National Park. Picture taken by Scott McGraw.

Figure 4. Strata levels in the Taï Forest, from McGraw 1998.

100% 90% 80% 70%

60% %Other 50% %Leaves 40% % Insects 30% % Fruit 20% 10% 0% Diana 1 Diana 2 Diana 3 Diana N Meta-diana group

Figure 5. Total group consumption of gross dietary components

Figure 6. The fruit of Dialium aubrevillei (Hawthorne and Gyakari 2006)

Figure 7. The seeds of Sacoglottis gabonensis (Hawthorne and Gyakari 2006)

Figure 8. The fruit of Scytopetalum tieghemii (Hawthorne and Gyakari 2006)

Figure 9. The fruit of Diospyros soubreana (Hawthorne and Jongkind 2006)

Figure 10. The fruit of Diospyros mannii (Hawthorne and Jongkind 2006).

Figure 11. The fruit of Parinari excelsa (Hawthorne and Gyakari 2006).

Figure 12. Leaves of Craterispermum caudatum (Hawthorne and Jongkind 2006)

60 Parinari excelsa

50 Oldfieldia africana

40 Craterispermum caudatum Diospyros mannii 30 Diospyros soubreana 20 Scytopetalum tieghemii 10 Sacoglottis gabonensis 0 Dialium aubrevillei

Figure 13. Total group consumption of the eight most frequently consumed plant parts.

100%

90%

80%

70%

60% %Other

50% %Leaves %Insects 40% %Fruit 30%

20%

10%

0% 2005 2006 2007 2008

Figure 14. Annual consumption of leaves, insects, fruits, and other dietary components from 2005-2008

50 Parinari excelsa

40 Oldfieldia africana Caterispermum caudatum

30 Diospyros mannii Diospyros soubreana 20 Scytopetalum tieghemii Sacoglottis gabonensis 10 Dialium aubrevillei

0 2005 2006 2007 2008

Figure 15. Annual consumption of the eight most frequently consumed plant parts

100%

90%

80%

70%

60% %Other

50% %Leaves

40% %Insect %Fruit 30%

20%

10%

0% Dry Season 1 Wet Season 1 Dry Season 2 Wet Season 2

Figure 16. Seasonal consumption of fruit, insects, leaves, and other material

70 Parinari excelsa

60 Oldfieldia africana

50 Caterispermum caudatum 40 Diospyros mannii

30 Diospyros soubreana

20 Scytopetalum tieghemii 10 Sacoglottis gabonensis

0 Dialium aubrevillei Wet Season 1 Dry Season 1 Wet Season 2 Dry Season 2

Figure 17. Seasonal consumption of the eight most frequently consumed plant parts

100.00

90.00

80.00

70.00

60.00 % Other 50.00 %Leaves % Insects 40.00 % Fruit 30.00

20.00

10.00

0.00 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Figure 18. Monthly consumption of fruit, insects, leaves, and other material.

100%

90%

80%

70%

60% %Other

50% %Leaves

40% %Insects %Fruit 30%

20% Rainfall 10%

0% Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Figure 19. Mean monthly rainfall and monthly consumption of fruit, insects, leaves, and other material during 2008

80 Parinari excelsa

70 Oldfieldia 60 africana Caterispermum 50 caudatum 40 Diospyros mannii 30 Diospyros 20 soubreana Scytopetalum 10 tieghemii 0 Sacoglottis gabonensis Dialium aubrevillei Figure 20. Monthly consumption of the eight most frequently consumed plant parts

80 Dialium aubrevillei 70

60 Sacoglottis gabonensis 50

30 Ripe fruit Unripe 20 fruit Ripe 10 Fruit Unripe Fruit 0 1 2 3 4 5 6 7 8 9 10 11 12

Figure 21. Monthly consumption and phenology of Sacoglottis gabonensis and Dialium aubrevillei

30 Ripe 25 Fruit

Unripe 20 Fruit

Scytopetalum 5 tieghemii

0 1 2 3 4 5 6 7 8 9 10 11 12

Figure 22. Monthly consumption and phenology of Scytopetalum tieghemii

15 Ripe fruit

10 Unripe fruit 5

0 1 2 3 4 5 6 7 8 9 10 11 12

Figure 23. Monthly consumption and phenology of Oldfieldia africana 59

5 Mature 4 leaves

3 Young 2 leaves

0 1 2 3 4 5 6 7 8 9 10 11 12

Figure 24. Monthly consumption and phenology of Craterispermum caudatum

20 18 16 14 12 10 Ripe 8 Fruit 6 4 Unripe 2 fruit 0 1 2 3 4 5 6 7 8 9 10 11 12

Figure 25. Monthly consumption and phenology of Parinari excelsa

Ripe fruit 10 Unripe…

0 1 2 3 4 5 6 7 8 9 10 11 12

Figure 26. Monthly consumption and phenology of Diospyros soubreana

Emergent Layer

Upper Canopy

Lower Canopy Fruit Insects Understory Leaves Saplings

Ground Level

0% 20% 40% 60% 80% 100%

Figure 27. Consumption of fruit, insect, and leaves in each forest strata

Emergent Dialium aubrevillei Layer Sacoglottis Upper gabonensis Canopy Scytopetalum Lower tieghemii Canopy Diospyros soubreana Diospyros mannii Understory

Craterispermum Saplings craudatum Oldfieldia africana

Ground Parinari excelsa

0 20 40 60 80 100

Figure 28. Consumption of eight most frequently consumed plant parts in each forest strata

100% 90% 80% 70% 60% Leaves 50% Insects 40% 30% Fruit 20% 10% 0% Adult Females Adult Males Subadults

Figure 29.Consumption of leaves, insects, and fruit by adult females, adult males, and subadults.

60 Parinari excelsa 50 Oldfieldia africana Craterispermum caudatum 40 Diospyros soubreana 30 Diospyros manii Scytopetalum tieghemii 20 Sacoglottis gabonensis 10 Dialium aubrevillei

0 Adult Females Adult Males Subadults

Figure 30. Consumption of eight most important plant parts by adult females, adult males, and subadults

100% 90% 80% 70% 60% Other 50% Leaves 40% Insects 30% Fruit 20% 10% 0% Contiguous groups North Group

Figure 31. Interdemic comparison of fruit, insects, leaf and other material consumption

Parinari excelsa 50 Oldfieldia africana

40 Craterispermum caudatum Diospyros mannii 30 Diospyros soubreana Scytopetalum tieghemii 20 Sacoglottis gabonensis Dialium aubrevillei 10

0 Contiguous groups North Group

Figure 32. Interdemic consumption of eight most frequently consumed plant parts.

100% 90% 80% 70% 60% Other 50% Leaves 40% 30% Insects 20% Fruit 10% 0% Tai 1970s Bia National Tiwai Island Tai 2000- Tai 2004- Park 1976- 1982-1984 2001 2009 1977

Figure 33. Consumption of fruit, insects, leaves, and other material by Diana monkeys at different sites across their range

100% 90% 80% 70% 60% Other 50% Leaves 40% Insects 30% Fruit 20% 10% 0% C. C. cephus C. C. C. mitis C. diana* ascanius pogonias nictitans

Figure 34 Proportion of fruit, insects, leaves, and other material in the diet of Cercopithecus diana and five other guenons (Chapman et al. 2002)

Figure 35. Fruit abundance in the Taï Forest between February 1997 and January 2000 (Anderson et al. 2005)

Emergent layer

Upper canopy Cling Feed Lower canopy Locomote Understory Rest Groom Sapling layer Social Play

Ground level

0% 20% 40% 60% 80% 100%

Figure 36. Frequency of behaviors performed at each level of the forest

Appendix B: Tables

Group Months Days Hours Scan Observations sampled sampled sampled Samples Diana 1 56 146 1,354 2,690 20,088 Diana 2 42 116 1,031.5 2,063 15,068 Diana 3 45 126 1,127.5 2,255 16,312 Diana N 44 122 1,011.5 2,023 14,316 Total 187 510 4,515.5 9,031 65,784 Table 1. Sampling effort over the duration of this study

Diana 1 Diana 2 Diana 3 Diana N Meta-Diana group Fruit 70.89 68.17 72.99 69.02 70.69 Insects 24.38 27.42 21.53 25.65 24.44 Leaves 4.29 3.90 5.22 5.15 4.46 Other 0.44 0.51 0.26 0.18 0.40 Table 2. Total group consumption of gross dietary components

Diana Diana Diana Diana Plant Parts Plant Type Total 1 2 3 N Dialium aubrevillei Ripe fruit 15.91 9.90 17.58 23.97 16.39 Sacoglottis gabonensis Ripe fruit 19.92 20.60 12.62 5.39 15.39 Scytopetalum tieghemii Ripe fruit 10.10 7.89 1.38 1.90 5.72 Diospyros soubreana Ripe fruit 5.53 8.26 4.71 1.23 5.17 Diospyros mannii Ripe fruit 3.15 5.47 5.97 5.30 4.88 Craterispermum caudatum Mature leaves 5.27 4.41 3.78 3.97 4.42 Oldfieldia africana Ripe fruit 5.61 1.53 4.97 3.43 3.98 Parinari excelsa Ripe fruit 2.20 4.45 3.94 3.22 3.41 Proportion of total diet 67.70 62.51 54.94 48.42 59.37

Table 3. Total group consumption of eight most frequently consumed plant parts

2005 2006 2007 2008 Fruit 75.52 71.14 62.32 72.20 Insects 20.43 21.06 32.71 24.78 Leaves 3.48 7.43 4.64 2.81 Other 0.57 0.37 0.33 0.21 Table 4. Annual consumption of fruit, insects, leaves, and other material from 2005- 2008.

Food type 2005 2006 2007 2008

Dialium aubrevillei Ripe fruit 22.36 6.11 26.61 14.01 Sacoglottis gabonensis Ripe fruit 9.90 25.46 7.36 17.53 Scytopetalum tieghemii Ripe fruit 5.16 0.23 0.48 0.64 Diospyros soubreana Ripe fruit 5.74 2.76 0.04 1.81 Diospyros mannii Ripe fruit 0.06 3.79 0.00 13.09 Caterispermum caudatum Mature leaves 2.39 4.85 4.42 2.63 Oldfieldia africana Ripe fruit 2.71 4.45 2.69 2.49 Parinari excelsa Ripe fruit 1.27 3.42 12.11 1.21 Table 5. Annual consumption of the eight most frequently consumed plant parts from 2005-2008

Wet Dry Wet Dry Season 1 Season 1 Season 2 Season 2 Dialium aubrevillei 25.86 3.11 0.07 17.89 Sacoglottis gabonensis 2.26 13.89 57.48 6.88 Scytopetalum tieghemii 8.96 6.58 - 0.07 Diospyros soubreana 0.10 - 0.07 11.72 Diospyros mannii 0.68 - - 8.01 Caterispermum caudatum 5.77 6.00 2.86 2.21 Oldfieldia africana 1.97 17.11 3.66 0.22 Parinari excelsa 1.49 - 0.04 7.04 Table 6. Seasonal consumpstion of eight most frequently consumed plant parts

% Fruit % Insects % Leaves % Other

January 83.61 14.87 1.45 0.08 February 74.85 21.70 3.33 0.12 March 71.00 25.31 3.17 0.52 April 53.39 33.90 12.29 0.42 May 65.32 28.06 6.36 0.26 June 68.37 24.30 7.09 0.24 July 63.49 28.68 7.60 0.24 August 66.63 27.37 5.90 0.10 September 79.03 17.49 2.70 0.79 October 69.79 26.25 3.80 0.16 November 69.43 26.83 3.05 0.70 December 54.79 44.81 0.20 0.20 Table 7. Monthly consumption of fruit, insects, leaves, and other material

Dialium Sacoglottis Scytopetalum Diospyros aubrevillei gabonensis tieghemii soubreana January 26.76 0.04 - 24.91 February 20.30 12.06 0.24 14.00 March 17.09 15.86 0.06 0.45 April 12.61 1.17 0.42 0.32 May 28.80 2.57 3.05 - June 31.75 2.65 24.60 0.08 July 5.01 0.94 10.54 - August - 35.20 0.10 - September - 69.56 - 0.07 October 0.16 42.65 - 0.08 November 0.61 5.14 - 0.09 December 7.63 - - - Diospyros Caterispermum Oldfieldia Parinari mannii caudatum africana excelsa January 12.70 1.41 - 2.81 February 3.94 3.09 - 10.42 March 13.20 2.91 1.04 17.22 April 2.33 6.67 0.11 6.46 May 0.32 5.25 1.68 - June - 5.95 1.93 - July - 5.30 8.78 - August - 4.55 19.73 - September - 2.56 5.46 0.07 October - 3.23 1.45 - November 0.17 2.61 - 0.70 December - 0.20 - - Table 8. Monthly consumption of eight most frequently consumed plant parts.

Fruit Insects Leaves

Ground Level 99.91 0.00 0.09 Saplings 58.57 4.81 36.62 Understory 55.14 38.94 5.92 Lower Canopy 64.13 34.56 1.31 Upper Canopy 84.15 15.75 0.11 Emergent Layer 75.54 24.21 0.24 Table 9. Consumption of fruit, leaves, and insects across forest strata.

Lower Upper Emergent Ground Saplings Understory Canopy Canopy Layer Dialium - - 0.07 22.98 26.75 - aubrevillei Sacoglottis 75.78 37.90 4.06 7.76 16.36 - gabonensis Scytopetalum - - - 10.55 - - tieghemii Diospyros - 3.77 22.67 0.62 0.04 - soubreana Diospyros 0.09 1.12 22.83 2.56 0.02 - mannii Craterispermum 0.09 35.58 6.73 0.34 - 0.24 craudatum Oldfieldia - - 0.03 1.85 8.26 6.30 africana Parinari 24.04 9.78 0.17 - 0.94 36.32 excelsa Table 10. Consumption of eight most frequently consumed plant parts across forest strata

Adult Females Adult Males Subadults

Fruit 61.60 66.79 68.55 Insects 31.82 30.09 24.17 Leaves 6.58 3.11 7.28 Table 11. Consumption of fruit, insects, and leaves by adult females, adult males, and subadults

Adult Females Adult Males Subadults

Dialium aubrevillei 10.02 10.09 10.77 Sacoglottis gabonensis 11.64 15.66 14.48 Scytopetalum tieghemii 7.69 5.57 10.38 Diospyros manii 6.86 5.66 5.73 Diospyros soubreana 6.79 3.58 5.99 Craterispermum caudatum 5.25 3.58 5.43 Oldfieldia africana 1.72 2.83 1.68 Parinari excelsa 3.10 5.00 4.09 Table 12. Consumption of eight most frequently consumed plant parts by adult females, adult males, and subadults

Contiguous Northern groups group Fruit 70.68 69.02 Insects 24.44 25.65 Leaves 4.47 5.15 Other 0.40 0.18 Table 13. Consumption of fruit, insects, leaves, and other material by the contiguous groups (Diana 1, Diana 2, Diana 3) and the northern group (Diana N)

Contiguous North groups Group Dialium aubrevillei 14.46 23.97 Sacoglottis gabonensis 17.71 5.39 Scytopetalum tieghemii 6.46 1.90 Diospyros soubreana 6.17 1.23 Diospyros mannii 4.86 5.30 Craterispermum caudatum 4.49 3.97 Oldfieldia africana 4.04 3.43 Parinari excelsa 3.53 3.22 Table 14. Consumption of the eight most frequently consumed plant parts by the contiguous groups (Diana 1, Diana 2, Diana 3) and the northern group (Diana N).

Study site Species Fruit Insects Leaves Other Tai C. d. diana 76.3 4 7.6 12.1 1970s Bia National Park C. d. roloway 20.9 33.8 6.5 38.8 1976-1977 Tiwai Island C. d. diana 26.52 27.65 12.55 33.28 1982-1984 Tai C. d. diana 59 16 16 9 2000-2001 Tai C. d. diana 70.43 24.66 4.6 0.31 2004-2009 * Table 15. Consumption of fruit, leaves, insects, and other material across Cercopithecus diana populations (Galat and Galat-Luong 1978, Oates and Whitesides 1990, Buzzard 2006, Curtin 2002, *this study)

Fruit Insects Leaves Other

C. ascanius 39.94 22.04 23.32 14.69 C. cephus 67.17 17.11 6.76 8.96 C. pogonias 57.57 11.11 6.65 24.67 C. nictitans 46.85 10.24 12.90 30.01 C. mitis 51.99 14.17 20.36 13.47 C. diana* 70.43 24.66 4.60 0.31 Table 16. Consumption of fruit, leaves, insects, and other material by multiple guenon species (Chapman et al. 2002, *this study).